Content uploaded by Tanja Schwander
Author content
All content in this area was uploaded by Tanja Schwander on Jul 03, 2018
Content may be subject to copyright.
Provided for non-commercial research and educational use.
Not for reproduction, distribution or commercial use.
This article was originally published in the Encyclopedia of Evolutionary Biology published by Elsevier, and the
attached copy is provided by Elsevier for the author’s benefit and for the benefit of the author’s institution, for non-
commercial research and educational use including without limitation use in instruction at your institution, sending
it to specific colleagues who you know, and providing a copy to your institution’s administrator.
All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing
copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited.
For exceptions, permission may be sought for such use through Elsevier’s permissions site at:
http://www.elsevier.com/locate/permissionusematerial
Jalvingh, K., Bast, J., and Schwander, T. (2016) Sex, Evolution and Maintenance of. In: Kliman, R.M. (ed.),
Encyclopedia of Evolutionary Biology. vol. 4, pp. 89–97. Oxford: Academic Press.
© 2016 Elsevier Inc. All rights reserved.
Sex, Evolution and Maintenance of
K Jalvingh, J Bast, and T Schwander, University of Lausanne, Lausanne, Switzerland
r2016 Elsevier Inc. All rights reserved.
Introduction
The ability to reproduce is one of the most fundamental as-
pects defining life, yet reproduction is achieved through a
panoply of mechanisms. Reproduction can involve different
levels of recombination and genetic exchange between indi-
viduals, ranging from clonal reproduction to meiotic par-
thenogenesis, self-fertilization or mating between relatives, to
sexual reproduction with outcrossing. Definitions of sex
therefore often depend on the context. A broad definition is
the joining of genetic material from two individuals to form
offspring that combine genes from both of them. If defined in
this way, sex is almost universal as it includes horizontal gene
transfers observed in prokaryotes and some eukaryotes, as well
as other types of 'parasexual'genetic exchange between indi-
viduals. A second definition of sex, the one adopted here, re-
fers to the formation of haploid gametes through meiosis,
followed by the fusion of these gametes (syngamy).
The evolution of sex combines two different topics; the
origin and the maintenance of sex. The origin of sex is highly
speculative as it happened during the early history of life on
Earth, when the first self-replicating RNA/DNA molecules ap-
peared. The single evolutionary origin of meiotic sex would
have occurred during this time, some 1.5 billion years ago.
There are different opinions concerning the mechanisms that
would have favored sex at its origin. For example, meiotic sex
could have been selected as a mechanism for DNA repair
(Bernstein et al., 1985). However, a more broadly accepted
view is that sex at its origin was favored through the same
mechanism that currently maintains it: it allows selection to
work efficiently. How exactly sex could facilitate selection is
explained below. Importantly, even small benefits conferred
by sex at its origin may have been enough. This is because
direct costs associated with sex at this time would have been
small since sex occurred between isogametic cells. By contrast,
sex has to generate strong benefits to be ‘maintained’under
anisogamy and biparental reproduction, the typical situation
in metazoans.
Sex is indeed associated with significant direct costs in
metazoans. In species where males provide little or no re-
sources to their offspring, females pay the full cost of repro-
duction, yet only provide half of each sexually produced
offspring’s genes. This generates a transmission disadvantage
relative to asexual reproduction, which is two-fold in species
that invest equally in both sexes (formalized by Maynard
Smith (1978) and Williams (1975)). Even in cases where
males do contribute resources to their offspring, sex is typically
still costly because it requires attracting mates and eventually
mating. These behaviors may be costly and increase risk of
predation or of infection with a sexually transmittable disease.
Sex can further cause reproductive failure if individuals fail
to find a mating partner. The paradox of sex –the fact that
it is associated with considerable costs but maintained in the
vast majority of organisms –thus stems in great part from a
metazoan-centered view.
Fitness effects of sex –the costs and benefits it generates –
can be expressed within populations (short-term con-
sequences) or at the lineage level (long-term consequences),
affecting the rate of adaptation, diversification, or extinction.
Within populations, sex can affect fitness directly or indirectly.
Direct fitness effects of sex are usually negative, for example,
the cost of males or costs related to mating. This means that
benefits of sex most likely stem from either indirect effects
on fitness or from long-term consequences. Long-term con-
sequences alone are probably insufficient to explain the
maintenance of sex, given the considerable direct costs of sex
(see Section Lineage-Level Selection For Sex). Indirect effects
on fitness arise when sex breaks up associations between al-
leles under selection (see Section Short-Term Benefits of Sex).
The intuitive idea that sex is good for the species was accepted
until the 1970s, when it was realized that there has to be a
gene-level advantage for sex and that this advantage has to be
strong enough to fully outweigh all the costs (Williams, 1975;
Maynard Smith, 1978). Therefore, there is an ongoing search
for strong short-term or individual-level benefits to explain the
maintenance of sex.
Short-Term Benefits of Sex
Sex generates indirect effects on fitness when it breaks up as-
sociations between alleles under selection. Much effort has
been invested into identifying situations where breaking up
such associations generates short-term fitness benefits. Before
examining situations where this might be the case, it is useful
to consider that for sex to have any indirect effect on fitness
(positive or negative), associations between selected alleles at
the same or at different loci need to exist in a population.
Without such linkage disequilibrium (LD), sex has no effect
(Figure 1).
Generating indirect benefits from breaking up LD requires
two mechanisms: (1) a mechanism that generates continuous
directional selection, for example, mutation or unceasing
changes in selection pressures. This is necessary to maintain
additive variance for fitness –in the absence of such variance,
there is no possibility for adaptation (and sex can thus not
facilitate it). (2) A mechanism that generates associations be-
tween genes with opposite ( and þ)fitness effects. If as-
sociations were between genes of identical fitness effects,
recombination would reduce the variance in fitness and
thereby slow down adaptation (Figure 2).
Identifying the mechanisms that generate continuous dir-
ectional selection is largely an empirical challenge, and these
mechanisms most likely vary among different organisms.
A general understanding of the advantage of sex therefore
requires understanding why associations between genes with
Encyclopedia of Evolutionary Biology, Volume 4 doi:10.1016/B978-0-12-800049-6.00144-X 89
Author's personal copy
AB
Genotype
Frequency
Genotype
Frequency
Genotype
Frequency
Genotype
Frequency
LD
No LD
Offspring
Parents
Sex
Sex
BBAA
AB BBAA AB BBAA
AB BBAA
Figure 1 Linkage Disequilibrium (LD). Under LD, there is a nonrandom association of alleles at different loci. If there is no LD in a population,
sex will have no effect. If there is LD, sex can generate new genotypes in the offspring that were not present in the parental population. Note that
LD concerns the frequency of genotypes in the population, not the frequency of individual alleles.
Chromosomes with
negative espistasis
After recombination
0–2 +2–1 +1
0–2 +2
–1 +1
Fitness
Frequency
Fitness distribution
Mutations:
Beneficial
Deleterious
Fitness
Frequency
0
–1
–1
+1
+1
–2
+2
0
0
0
0
Figure 2 Negative epistasis. In the presence of negative epistasis, interactions between alleles reduce or reinforce fitness effects. Under negative
epistasis, sex can generate benefits by breaking up LD and thereby increasing fitness variance, which will improve the response to selection.
90 Sex, Evolution and Maintenance of
Author's personal copy
opposite fitness effects should be predominant. The four best
studied mechanisms that could generate such associations are:
Epistasis
If the effect of a locus on fitness depends on other loci (i.e., if
there is epistasis), selection systematically generates LD. If
epistasis is generally negative, sex would be favored because it
would increase fitness variance in the next generation (Barton,
1995). Because fitness variance increases, recombination pro-
vides a benefit by increasing the response to selection. In
addition to this benefit, recombination also generates a cost.
This cost stems from the fact that LD was generated by selec-
tion, meaning that recombination breaks up good gene com-
binations and generates worse ones. This ‘recombination load’
causes an immediate reduction of mean fitness, which has to
be compensated by the benefit of the increased response to
selection. As a consequence, for recombination with negative
epistasis to generate a net benefit, epistasis cannot be strongly
negative or the costs due to the recombination load would be
too high (Otto and Feldman, 1997). The current empirical
evidence indicates that epistasis is generally not negative
(Elena and Lenski, 1997;De Visser and Elena, 2007). This
implies that negative epistasis is unlikely to be a main driver in
the evolution and maintenance of sex.
Temporal Changes in Selection
Epistasis can generate a short-term advantage for recombin-
ation when it fluctuates over time, with different allele com-
binations being favored during different time intervals
(Maynard Smith, 1971;Charlesworth, 1976;Barton, 1995).
The evolution of recombination requires that these time
intervals are quite short (a few generations), which is perhaps
most likely if fluctuating epistasis is caused by interactions
between coevolving species (Peters and Lively, 1999;Gandon
and Otto, 2007).
Much research effort has been dedicated to the study of
coevolution, especially between hosts and parasites. In the
context of Red Queen dynamics, a parasite would adapt to the
most common host genotype, because it can then infect many
hosts. In this situation, a rare host genotype would be favored,
causing its frequency to increase until it becomes common
(negative frequency-dependent selection). Parasites should
then shift to infect this newly common genotype, reducing its
fitness in the current generation. There is accumulating
evidence for Red Queen dynamics in natural populations and
from experimental evolution (e.g., Lively, 1987;Decaestecker
et al., 2007;Morran et al., 2011). However, whether these
dynamics contribute to the maintenance of sex in many spe-
cies remains unknown. For example, negative frequency-
dependent selection does not require sex but can also work
in asexual species consisting of a genetically diverse assem-
blage of clones. In that case, negative frequency-dependent
fitness of different clones would act to maintain clonal diver-
sity rather than sex. Furthermore, there are several examples
where parasites appear to not contribute to the maintenance
of sex (e.g., Parker, 1994;Hanley et al., 1995;Elzinga et al.,
2012).
Migration and Spatial Changes in Selection
Spatial variation in selection can generate locally adapted al-
lele associations with locally maladapted associations intro-
duced by migration. Sex can then provide a benefit because it
breaks such maladaptive allele associations, provided migra-
tion rates are high enough to regularly introduce locally
maladapted associations, yet low enough to not constrain
local adaptation via gene flow (Agrawal, 2009;Lenormand
and Otto, 2000;Pylkov et al., 1998). These theoretical pre-
dictions were supported by results from an experimental
evolution approach in cyclically parthenogenetic rotifers. By
controlling migration rates between similar and different
rearing environments, Becks and Agrawal (2010) showed that
higher rates of sex are maintained under migration between
different environments.
However, potential benefits for sex under spatially hetero-
geneous selection depend on the specific conditions. For ex-
ample, selected alleles should be dominant under conditions
where they are beneficial, and recessive under conditions
where they are maladaptive (Agrawal, 2009). Furthermore,
depending on the correlation in selection on different loci
across populations, migration can generate either positive or
negative linkage disequilibria across loci (Lenormand and
Otto, 2000).
Drift and the Hill–Robertson Effect
In finite populations, negative LD between loci under selection
is generated by the combined effects of drift and selection.
Drift generates all possible types of LD between loci under
selection: associations between beneficial alleles, associations
between deleterious alleles, and associations between alleles
with opposite fitness effects. Selection acts efficiently on the
first two categories, given the big fitness differences they gen-
erate. This means that most cases of LD that persist after se-
lection are due to associations between alleles with opposite
fitness effects (Hill and Robertson, 1966). This so called ‘Hill–
Robertson effect’favors sex because breaking up associations
between alleles with opposite fitness effects increases the
variance in fitness (Felsenstein, 1974; see also Figure 2).
Since natural populations (at least of macroorganisms) are
typically within the size range where Hill–Robertson effects
can generate benefits for sex, drift generates perhaps the most
broadly applicable benefits for sex. However, it remains un-
known to what degree such benefits can compensate for the
direct costs associated with sex.
In summary, breaking up associations between alleles at
different loci can provide an advantage for sexual over asexual
reproduction when these associations hamper adaptation, as is
often the case within finite populations, or when selection
varies over time or space. Whether such indirect benefits of sex
may be sufficient to outweigh the direct costs remains un-
known. Furthermore, for obtaining benefits from reducing
associations between loci, even very rare events of sex are
sufficient. The presented models do therefore not explain
the prevalence of obligate sex with high recombination rates
(Hurst and Peck, 1996). There is currently no LD-based hy-
pothesis that can account for obligate sex, the most widespread
form of reproduction among metazoans.
Sex, Evolution and Maintenance of 91
Author's personal copy
Short-term benefits of sex not related to linkage
disequilibria
A specific form of spatial variation in selection is at the root of
some of the classical, ecology-based models proposing benefits
to sex, which include the ‘Tangled Bank’model (e.g., Ghiselin,
1974;Maynard Smith, 1978;Bell, 1982;Song et al., 2011).
These models posit that there is genetically based variation
among individuals for exploiting different niches. As a con-
sequence, genetically identical individuals should experience
more intense competition than genetically different indi-
viduals. Here, sex could provide benefits because sexually
produced offspring would display more genetic variation than
asexually produced ones. The ‘Tangled Bank’concept thus
proposes an advantage for sex in environments that are sat-
urated, as sex would reduce sibling competition in this case.
Some recent extensions of the ‘Tangled Bank’(Song et al.,
2011) work in similar ways to negative frequency-dependent
selection under host–parasite coevolution. Here, the availability
of resources depends on the frequency at which these resources
are exploited and replaced. If different genotypes exploit differ-
ent resources, rare genotypes will be favored because they use a
resource that is temporarily abundant.
Lineage-Level Selection for Sex
As explained above, meiotic sex has evolved once and has been
maintained in the vast majority of lineages on the tree of life.
This means that current asexual lineages derive secondarily
from sexual ancestors. It has been argued that only those
sexual lineages that cannot give rise to new asexuals (due to
genetic or developmental constraints) persist in the long-term
(Williams, 1975;Nunney, 1989). Sexual lineages without
constraints would be driven to extinction by the asexuals they
generate.
Several hypotheses further propose long-term disadvan-
tages to asexual reproduction. For example, 'Muller's ratchet'
describes the pattern where small populations of asexual lin-
eages tend to accumulate deleterious mutations over time
(Muller, 1964). Clones can be lost from small populations as a
consequence of drift, including the clones with the fewest
deleterious mutations. New deleterious mutations are intro-
duced during replication, such that the average number of
deleterious mutations per clone in an asexual population can
only increase over time, in a ratchet-like manner (hence the
term Muller's ratchet). Small sexual populations also lose
genotypes as a consequence of drift. However, via recombin-
ation and mixis, sex can regenerate mutation-free genotypes
and thereby avoid the ratchet.
The ‘lottery model’compares sexual and asexual repro-
duction to different strategies when buying lottery tickets
(Williams, 1975). Asexuality corresponds to buying many
tickets with the same number, while sexual reproduction
corresponds to buying tickets with different numbers. The
expected payoff of the two strategies is similar, but the payoff
variance should be greater for asexuals, with the consequence
Figure 3 Overview of the different reproductive modes described in the text. Sexual reproduction with or without spontaneous parthenogenesis. In
sexually reproducing species, offspring contain the genetic material of the father and mother. Sexual reproduction involves meiosis and
recombination, both of which may also be present at some level in alternative modes of reproduction. In some cases, spontaneous parthenogenesis
(also called tychoparthenogenesis or accidental parthenogenesis) occurs under sexual reproduction when virgin females are able to produce viable
offspring. All known cases of spontaneous parthenogenesis are meiotic. It is widespread among invertebrates and has also been documented in some
vertebrate species, especially in species kept in zoos. Spontaneous parthenogenesis is sometimes called ‘facultative parthenogenesis’although
hatching success under spontaneous parthenogenesis, rarely higher than 1% and often as low as 0.1%, is typically more than an order of magnitude
lower than under facultative parthenogenesis, where the majority of unfertilized eggs hatch. Sperm-dependent parthenogenesis: it (also called
gynogenesis, pseudogamy or sperm parasitism) is a parthenogenesis in which the egg needs to be activated by sperm for embryogenesis to start.
Thus as under other types of parthenogenesis, there is no paternal contribution (genetic or cytoplasmic) to the offspring. Sperm-dependent
parthenogens derive from sexual ancestors where egg activation is already sperm-dependent, possibly because egg–sperm interactions may function
as a control mechanism preventing the unwarranted development of eggs prior to fertilization. Sperm-dependent parthenogenetic lineages must
coexist with their ‘sperm donors,’usually males (or hermaphroditic individuals) from a related sexual species or population. Although rare, sperm-
dependent parthenogenesis has been reported in a wide variety of animal taxa, including vertebrate and invertebrate taxa. Mating systems like these
are potentially unstable, since they depend on the sperm from an individual who cannot gain paternity in return. Cyclical parthenogenesis: it is the
alternation between a generation of sexual reproduction and one or more generations of asexual reproduction in a single population. During the
parthenogenetic generations, females only produce daughters, except for the last generation, preceding the sexual generation. Prior to the sexual
generation, females produce sons in addition to daughters. These parthenogenetically produced males and females mate, and the female offspring
from these crosses are the first parthenogenetic generation of the next cycle. The parthenogenetic generations are generally mitotically produced
(i.e., clonal). The parthenogenetic production of males is achieved via different developmental processes in different species, depending on theirsex
determination mechanism. In species with environmental sex determination (e.g., in water fleas) male differentiation is induced by specificabiotic
conditions. In species with haplodiploid sex determination (e.g., in rotifers or cynipids) females start laying haploid eggs, while in species with other
genetic sex determination systems, male development involves complex processes of sex chromosome elimination (as Wilson et al., 1997 described
for aphids). Obligate Parthenogenesis: parthenogenesis in animals often refers to the production of daughters without genetic contributions from
males (‘female-producing parthenogenesis’or thelytoky). Under obligately parthenogenesis all individuals only reproduce via parthenogenesis: the
ability to produce offspring with genetic contributions from males has been lost. Both obligate meiotic and mitotic asexual reproduction falls under
this definition. Mixed reproduction: in mixed reproduction a population consists of both sexually and asexually reproducing individuals. Crucially,
each individual reproduces either sexually or asexually, and is not able to alternate between reproductive modes, making it functionally distinctive
from both cyclical and facultative parthenogenesis. Hermaphroditism: these are organisms that combine male and female functions within the same
individual. In some cases, hermaphrodites are able to fertilize their own eggs, making them functionally asexual, even though the fusion of gametes
still occurs. Facultative parthenogenesis: in lineages with facultative parthenogenesis, reproduction can be through biparental sex and through
female-producing parthenogenesis. Facultatively parthenogenetic females can flexibly shift between the two reproductive modes and parthenogenesis
is generally meiotic.
92 Sex, Evolution and Maintenance of
Author's personal copy
that asexual lineages should face higher extinction rates than
sexual ones.
Sexual and asexual lineages are also expected to differ
in their long-term rate of adaptation, i.e., the ‘classical’
explanation for the benefits of sex. According to the Fisher–
Muller hypothesis, sexual lineages adapt faster, because
beneficial mutations occurring in different individuals can be
combined in one (Fisher, 1930;Muller, 1932). In an asexual
Sexual reproduction Parthenogenesis
Sperm dependent parthenogenesis
Sexual reproduction
with accidental parthenogenesis
Mixed reprodutionHermaphroditism
Facultative parthenogenesis Cyclical parthenogenesis
Sex, Evolution and Maintenance of 93
Author's personal copy
lineage, the same beneficial mutations must be fixed sequen-
tially. If different beneficial mutations appear simultaneously
in different individuals, competition among such mutations
('clonal interference,’Muller, 1932;Gerrish and Lenski, 1998)
can slow the rate of adaptation (and theoretical fitness optima
may never be reached).
Although intuitively appealing, long-term mechanisms are
unlikely to explain the maintenance of sex in the bulk of
species. For example, they do not apply under very large
population sizes, which are characteristic of many micro-
organisms. This is because all combinations of beneficial and
deleterious mutations appear at their expected frequencies in
infinite populations, and recombination confers no advantage.
Furthermore, such arguments cannot explain the maintenance
of sex in lineages characterized by sexual and asexual repro-
duction (i.e., in lineages with facultative parthenogenesis,
cyclical parthenogenesis, or mixed reproduction): here, sex
must confer benefits on a sufficiently short timescale so that its
direct costs can be outweighed.
The Diversity and Taxonomic Distribution of
Reproductive Modes
The level of sex can vary continuously among reproductive
modes, from its complete lack in mitotic forms of par-
thenogenesis to obligate sex between unrelated individuals
(Figure 3). Female-producing parthenogenesis (‘thelytoky’)
occurs in different forms –it can be cyclical, facultative, acci-
dental, or obligate. Cyclical parthenogenesis (also called
heterogony) is a type of life cycle in which a sexual generation
(bisexual or hermaphroditic) alternates with one or more
generations of parthenogenetic reproduction. Six large animal
groups are characterized by this life cycle: trematodes
(a parasitic class of flatworms), rotifers, cladocerans (water
fleas such as Daphnia), aphids (including adelgids, and phyl-
loxerids), cecidomyiids (gall midges), and cynipids (gall
wasps). Parthenogenesis typically predominates under favor-
able conditions; deteriorating or stressful conditions (e.g.,
linked to seasonality, resource depletion and/or crowding)
trigger the production of males and sexual females. Cyclical
parthenogens frequently generate strains characterized by ob-
ligate parthenogenesis in which the sexual cycle can no longer
be induced. This is well documented for several strains of
aphids and water fleas (Dedryver et al., 2013;Tucker and
Ackerman, 2013;Neiman et al., 2014).
Similar to cyclical parthenogenesis, facultative partheno-
genesis characterizes lineages that can use both biparental sex
and female-producing parthenogenesis to generate offspring.
In contrast to cyclical parthenogens, facultatively partheno-
genetic females can flexibly shift between the two reproductive
modes and parthenogenesis is generally meiotic while it is
mitotic (i.e., clonal) in cyclical parthenogens. The efficiency of
parthenogenesis and sexual reproduction (number of offspring
produced) is comparable under facultative parthenogenesis,
distinguishing it from spontaneous parthenogenesis in
sexual species. However, survival rates are typically higher
for sexually than parthenogenetically produced offspring
such that, given the option, females will prefer to produce
sexual rather than parthenogenetic offspring. Facultative
parthenogenesis occurs and may be widespread in some insect
groups such as phasmids, mayflies, or termites, but is most
likely rare in other animal groups. More frequent is mixed
reproduction (species with sexual and parthenogenetic
strains) however females in each strain are obligately sexual or
obligately parthenogenetic.
In summary, most types of female-producing partheno-
genesis would avoid certain indirect and direct costs associated
with sexual reproduction, including the breaking up of coa-
dapted gene complexes, the production of sons as well as costs
involved in mate finding and copulation. In this context fe-
male-producing parthenogenesis is often used interchangeably
with asexuality, although parthenogenesis does not necessarily
generate clones. Many forms of parthenogenesis involve mei-
osis whereby ploidy levels (reduced during meiosis) are
maintained between generations via specific cell regulatory or
developmental mechanisms that act before, during or after the
meiotic divisions (Suomalainen et al., 1987).
Among animals, female-producing parthenogenesis has
been estimated to occur in approximately 1 in a 1000 species
(Vrijenhoek, 1998). However, this estimate is largely based on
vertebrates and ignores several species-rich groups with large
proportions of parthenogenetic lineages (e.g., hymenopterans
and mites). True proportions of lineages capable of par-
thenogenesis may be up to an order of magnitude higher. The
incidence of parthenogenesis varies widely among groups;
classic examples of the extremes are mammals and birds
without any parthenogenetic species, and cyclical partheno-
gens where parthenogenetic generations are part of an every
species’live cycle.
Evolution of Parthenogenesis from Sexual Ancestors
In species that are not cyclical or facultative parthenogens, the
evolution of a transition to parthenogenesis is most likely
complex, requiring the acquisition of multiple novel adap-
tations (such as diploid instead of haploid gametes and
spontaneous gamete development without sperm contri-
bution (Neiman et al. 2014)). In addition to mutations, at
least three different mechanisms can generate new partheno-
genetic lineages from bisexual ancestors. First, hybridization
between two sexual species has generated many described
parthenogenetic lineages, and notably all but one known
vertebrate parthenogen (Avise, 2008). The overall frequency of
hybrid species among invertebrate parthenogens remains to be
estimated. The cause of the association between partheno-
genesis and hybridization remains largely unknown but may
have different origins in different taxa. In some cases hybrid-
ization per se induces parthenogenesis. Under the 'balance
hypothesis'(Moritz et al., 1989) parthenogenesis via hybrid-
ization can only arise when the genomes of parental species
are divergent enough to disrupt meiosis in hybrids, yet not so
divergent as to compromise hybrid viability or fertility. In
other cases, it has been hypothesized that parthenogens of
hybrid origin have better competitive abilities relative to sexual
sister species than non-hybrid parthenogens (Innes and
Hebert, 1988).
Second, in some species, parthenogenesis is induced by
infection with endosymbionts such as the bacteria Wolbachia
94 Sex, Evolution and Maintenance of
Author's personal copy
and Cardinium (reviewed in Duron et al., 2008). Thus far,
parthenogenesis induction by endosymbionts has only
been experimentally confirmed in species with haplodiploid
sex determination (notably in wasps, thrips and mites;
reviewed in Neiman et al., 2014). However, there are at
least two species with other sex determination systems (the
springtail Folsomia candida and the hemipteran Aspidiotus
nerii (Pike and Kingcombe, 2009;Provencher et al., 2005))
with a strong correlation between parthenogenesis and endo-
symbiont infection.
Finally, in some parthenogenetic lineages, females produce
males that, by mating with females of related sexual lineages,
generate new parthenogenetic lineages. This process is referred
to as ‘contagious parthenogenesis’because gene flow from
parthenogenetic into sexual lineages could allow for the spread
of parthenogenesis-causing elements in a contagious fashion
(Jaenike and Selander, 1979). In some cyclical parthenogens
(especially Daphnia and aphids), the spread of obligate par-
thenogenesis is indeed at least partly mediated by such gene
flow. However, despite the high potential of this contagious
mechanism to generate parthenogenetic lineages, its incidence
in natural populations is unknown, and may be limited since
the geographic distribution ranges of sexual and partheno-
genetic relatives are often distinct.
Sometimes polyploidy is hypothesized to cause partheno-
genesis because it is more widespread among parthenogenetic
as compared to sexual animals (Otto and Whitton, 2000). It is
unclear whether polyploidy per se can induce parthenogenesis
or whether the evolution of parthenogenesis and polyploidy
are generally independent events. Some polyploid partheno-
gens derive from diploid ones via rare fertilization of par-
thenogenetic eggs but it is not known how widespread this
mechanism is. There is also a lack of broad estimates of
polyploidy incidence among parthenogens. Estimates based
on small numbers of taxa are unreliable as the incidence
of polyploidy varies widely among groups. For example,
while the parthenogenetic beetles in the weevil family are
generally polyploid, the numerous parthenogenetic hymen-
opteran and mite lineages are diploid. In cases where par-
thenogens are polyploid, polyploidy is likely to play a major
role in the persistence of sex versus parthenogenesis as it can
affect ecology and life-history traits (Otto and Whitton, 2000)
and delays the expression of recessive deleterious alleles
(Archetti, 2010).
Empirical Evidence for Benefits of Sex
Three different empirical approaches can be used to identify
benefits of sex, each with specific advantages and disadvan-
tages. The first set of approaches measures fundamental par-
ameters used in evolutionary models predicting benefits of sex:
epistasis (reviewed in De Visser and Elena, 2007) or rates of
genomic mutations and the distributions of their fitness effects
(e.g., Haag-Liautard et al., 2007;Lynch et al., 2008;Ossowski
et al., 2010).
A second set of approaches relies on experimental evolution
to test whether mechanisms predicted to favor sex in theoretical
studies apply to real organisms. These approaches have shown,
for example, that sex speeds up adaptation to new
environments in microorganisms (Colegrave, 2002;Poon and
Chao, 2004;Goddard et al.,2005;Grimberg and Zeyl, 2005;
Cooper, 2007) and that higher rates of sex are maintained
during adaptation in cyclical parthenogens and facultatively
selfing macroorganisms (Morran et al.,2009;Becks and Agra-
wal, 2012). These studies thus provide a ‘proof-of-principle’that
theoretically predicted mechanisms can favor sex given the ap-
propriate conditions. However, these conditions may not be
realized in natural populations, such that experimental evo-
lution does not provide insights into the maintenance of sex in
natural populations. Indeed, it is impossible to know whether
any benefit to sex detected under artificial conditions (that may
include controlled migration rates, specific population densities
or sizes) would outweigh its immediate costs expressed under
natural conditions.
Finally, a third empirical approach involves field studies
and comparisons of asexual and related sexual lineages. While
such studies provide insights into mechanisms important in
natural populations, they generally remain correlational. Fur-
thermore, when benefits of sex are identified in natural
populations, it is often difficult to disentangle through which
mechanisms such benefits are generated.
One of the best-documented consequences of sexual re-
production in natural populations is that it facilitates the
purging of deleterious mutations. Thus, an increase of puta-
tively deleterious (i.e., coding) mutations under asexual re-
production has been shown in a number of studies, both in
animals (e.g., molluscs (Johnson and Howard, 2007;Neiman
et al., 2010), stick insects (Henry et al., 2012), Daphnia (Paland
and Lynch, 2006; but see Tucker and Ackerman, 2013)) and
plants (e.g., Oenothera primroses; Hollister et al., 2014). The
extent to which the accumulation of such coding mutations
results in negative phenotypic effects remains unknown. Fur-
thermore, deleterious mutation accumulation would generate
lineage-level (long-term) selection for sex, which, as explained
above is insufficient to maintain sex in most cases.
Host–parasite coevolutionary dynamics can drive the con-
stantly changing conditions required to generate persisting
benefits for sex. Accordingly, some of the strongest evidence
for benefits of sex in natural populations stems from host–
parasite dynamics. In natural populations of New Zealand
freshwater snails (Potamopyrgus antipodarum), sexually repro-
ducing snails are favored in lakes and microhabitats within
lakes with low prevalence of trematode parasites while asexual
snails tend to occur in lakes or microhabitats where parasites
are rare (Lively, 1987;King et al., 2011). Whether parasites are
the main driver to maintain sex in natural populations re-
mains however unclear, as similar evidence lacks for other
systems of co-occurring sexual and asexual lineages or even
shows benefits for asexuals (e.g., Parker, 1994;Hanley et al.,
1995;Elzinga et al., 2012).
Correlational evidence from natural populations is further
consistent with Tangled-Bank related mechanisms favoring
sex. Relative to asexual mite species, sexual species occupy
higher trophic levels and occur in habitats where resource
availability is more limited (Fischer et al., 2014). Furthermore,
high proportions of sexually reproducing mites are found in
locations with low population densities, suggesting that sexual
reproduction is favored under resource-limiting conditions
(Maraun et al., 2012).
Sex, Evolution and Maintenance of 95
Author's personal copy
Conclusion
Sophisticated theoretical approaches have generated insights
into the mechanisms through which sex could favor adap-
tation. However, it remains unknown whether any of the
identified mechanisms (or all of them combined) is able to
generate sufficiently strong selection for sex to be maintained
in natural populations, that is, fully compensate the costs ex-
pressed under these conditions.
Although many of the predicted benefits of sex have at least
some empirical support, the benefits and costs of sex might
vary among species. For example, physiological and develop-
mental constraints on asexual reproduction, levels of eco-
logical differentiation within a species and different life-history
traits can all affect the relative costs and benefits of sex
(Meirmans et al., 2012). Consequently, the maintenance of sex
in natural populations has most likely strong lineage-specific
components. The implications are that there might be no
single universal theory that can explain sexual reproduction in
all systems (West et al., 1999).
See also: Mating Systems, A Brief History of. Recombination and
Molecular Evolution. Recombination and Selection. Sex
Chromosome Evolution: Birth, Maturation, Decay, and Rebirth. Sex
Determination
References
Agrawal, A.F., 2009. Spatial heterogeneity and the evolution of sex in diploids.
American Naturalist 174, S54–S70.
Archetti, M., 2010. Complementation, genetic conflict, and the evolution of sex and
recombination. Journal of Heredity 101, 21–33.
Avise, J.C., 2008. Clonality: The Genetics, Ecology, and Evolution of Sexual
Abstinence in Vertebrate Animals. Oxford: Oxford University Press.
Barton, N.H., 1995. Linkage and the limits to natural selection. Genetics 140,
821–841.
Becks, L., Agrawal, A.F., 2010. Higher rates of sex evolve in spatially heterogeneous
environments. Nature 468, 89–92.
Becks, L., Agrawal, A.F., 2012. The evolution of sex is favoured during adaptation to
new environments. PLoS Biology 10, e1001317.
Bell, G., 1982. The Masterpiece of Nature: The Evolution and Genetics of Sexuality.
Los Angeles, CA: University of California Press.
Bernstein, H., Byerly, H.C., Hopf, F.A., Michod, R.E., 1985. Genetic damage,
mutation, and the evolution of sex. Science 229, 1277–1281.
Charlesworth, B., 1976. Recombination modification in a fluctuating environment.
Genetics 83, 181–195.
Colegrave, N., 2002. Sex releases the speed limit on evolution. Nature 420,
664–666.
Cooper, T.F., 2007. Recombination speeds adaptation by reducing competition
between beneficial mutations in populations of Escherichia coli. PLoS Biology 5,
1899–1905.
Decaestecker, E., Gaba, S., Raeymaekers, J.A.M., et al., 2007. Host−parasite Red
Queen dynamics archived in pond sediment. Nature 450, 870–873.
Dedryver, C., Le Gallic, J.-F., Mahéo, F., Simon, J.-C., Dedryver, F., 2013. The
genetics of obligate parthenogenesis in an aphid species and its consequences
for the maintenance of alternative reproductive modes. Heredity 110, 39–45.
Duron, O., Bouchon, D., Boutin, S., et al., 2008. The diversity of reproductive
parasites among arthropods: Wolbachia do not walk alone. BMC Biology 6, 27.
Elena, S.F., Lenski, R.E., 1997. Test of synergistic interactions among deleterious
mutations in bacteria. Nature 390, 395–398.
Elzinga, J.A., Chevasco, V., Mappes, J., Grapputo, A., 2012. Low parasitism rates in
parthenogenetic bagworm moths do not support the parasitoid hypothesis for
sex. Journal of Evolutionary Biology 25, 2547–2558.
Felsenstein, J., 1974. The evolutionary advantage of recombination. Genetics 78,
737–756.
Fischer, B.M., Meyer, E., Maraun, M., 2014. Positive correlation of trophic
level and proportion of sexual taxa of oribatid mites (Acari: Oribatida) in alpine
soil systems. Experimental and Applied Acarology 63, 465–479.
Fisher, R.A., 1930. The Genetical Theory of Natural Selection. Oxford: Clarendon
Press.
Gandon, S., Otto, S.P., 2007. The evolution of sex and recombination in response to
abiotic or coevolutionary fluctuations in epistasis. Genetics 175, 1835–1853.
Gerrish, P.J., Lenski, R.E., 1998. The fate of competing beneficial mutations in an
asexual population. Propagation of Ornamental Plants 102/103, 127–144.
Ghiselin, M.T., 1974. The Economy of Nature and the Evolution of Sex. Los
Angeles, CA: University of California Press.
Goddard, M.R., Godfray, H.C.J., Burt, A., 2005. Sex increases the efficacy of natural
selection in experimental yeast populations. Nature 434, 636–640.
Grimberg, B., Zeyl, C., 2005. The effects of sex and mutation rate on adaptation in
test tubes and to mouse hosts by Saccharomyces cerevisiae. Evolution 59,
431–438.
Haag-Liautard, C., Dorris, M., Maside, X., et al., 2007. Direct estimation of per
nucleotide and genomic deleterious mutation rates in Drosophila.Nature445,82–85.
Hanley, K.A., Fisher, R.N., Case, T.J., 1995. Lower mite infestations in an asexual
gecko compared with its sexual ancestors. Evolution 49, 418–426.
Henry, L., Schwander, T., Crespi, B.J., 2012. Deleterious mutation accumulation in
asexual Timema stick insects. Molecular Biology and Evolution 29, 401–408.
Hill, W.G., Robertson, A., 1966. The effect of linkage on limits to artificial selection.
Genetical Research 8, 269–294.
Hollister, J.D., Greiner, S., Wang, W., et al., 2014. Recurrent loss of sex is
associated with accumulation of deleterious mutations in Oenothera. Molecular
Biology and Evolution 32, 896–905.
Hurst, L.D., Peck, J.R., 1996. Recent advances in understanding of the evolution and
maintenance of sex. Trends in Ecology and Evolution 11, 46–52.
Innes, D.J., Hebert, P.N.D., 1988. The origin and genetic basis of obligate
parthenogenesis in Daphnia pulex. Evolution 42, 1024–1035.
Jaenike, J., Selander, R.K., 1979. Evolution and ecology of parthenogenesis in
earthworms. American Zoologist 19, 729–737.
Johnson, S.G., Howard, R.S., 2007. Contrasting patterns of synonymous and
nonsynonymous sequence evolution in asexual and sexual freshwater snail
lineages. Evolution 61, 2728–2735.
King, K.C., Jokela, J., Lively, C.M., 2011. Parasites, sex, and clonal diversity in
natural snail populations. Evolution 65, 1474–1481.
Lenormand, T., Otto, S.P., 2000. The evolution of recombination in a heterogeneous
environment. Genetics 156, 423–438.
Lively, C.M., 1987. Evidence from a New Zealand snail for the maintenance of sex
by parasitism. Nature 328, 519–521.
Lynch, M., Sung, W., Morris, K., et al., 2008. A genome-wide view of the spectrum
of spontaneous mutations in yeast. Proceedings of the National Academy of
Sciences of the United States of America 105, 9272–9277.
Maraun, M., Norton, R.A., Ehnes, R.B., Scheu, S., Erdmann, G., 2012. Positive
correlation between density and parthenogenetic reproduction in oribatid mites
(Acari) supports the structured resource theory of sexual reproduction.
Evolutionary Ecology Research 14, 311–323.
Maynard Smith, J., 1971. The origin and maintenance of sex. In: Williams, G.C.
(Ed.), Group Selection. Chicago, IL: Aldine Atherton, pp. 163–175.
Maynard Smith, J., 1978. The Evolution of Sex. New York, NY: Cambridge
University Press.
Meirmans, S., Meirmans, P.G., Kirkendall, L.R., 2012. The costs of sex: Facing real-
world complexities. Quarterly Review of Biology 87, 19–40.
Moritz, C.C., Brown, W.M., Densmore, L.D., et al., 1989. Genetic diversity and the
dynamics of hybrid parthenogenesis in Cnemidophorus (Teiidae) and Heteronotia
(Gekkonidae). In: Dawley, R.M., Bogart, J.P. (Eds.), Evolution and Ecology of
Unisexual Vertebrates. New York, NY: University of the State of New York,
pp. 87–112.
Morran, L.T., Parmenter, M.D., Phillips, P.C., 2009. Mutation load and rapid
adaptation favour outcrossing over self-fertilization. Nature 462, 350–352.
Morran, L.T., Schmidt, O.G., Gelarden, I.A., Parrish, R.C., Lively, C.M., 2011.
Running with the Red Queen: Host−parasite coevolution selects for biparental
sex. Science 333, 216–218.
Muller, H.J., 1932. Some genetic aspects of sex. American Naturalist 66, 118–138.
Muller, H.J., 1964. The relation of recombination to mutational advance. Mutation
Research 1, 2–9.
Neiman, M., Hehman, G., Miller, J.T., Logsdon, J.M., Taylor, D.R., 2010.
Accelerated mutation accumulation in asexual lineages of a freshwater snail.
Molecular Biology and Evolution 27, 954–963.
96 Sex, Evolution and Maintenance of
Author's personal copy
Neiman, M., Sharbel, T.F., Schwander, T., 2014. Genetic causes of transitions from
sexual reproduction to asexuality in plants and animals. Journal of Evolutionary
Biology 27, 1346–1359.
Nunney, L., 1989. The maintenance of sex by group selection. Evolution 43, 245–257.
Ossowski, S., Schneeberger, K., Lucas-Lledó, J.I., et al., 2010. The rate and
molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science
327, 92–94.
Otto, S.P., Feldman, M.W., 1997. Deleterious mutations, variable epistatic
interactions, and the evolution of recombination. Theoretical Population Biology
51, 134–147.
Otto, S.P., Whitton, J., 2000. Polyploidy incidence and evolution. Annual Review of
Genetics 34, 401–437.
Paland, S., Lynch, M., 2006. Transitions to asexuality result in excess amino acid
substitutions. Science 311, 990–992.
Parker, M.A., 1994. Pathogens and sex in plants. Evolutionary Ecology 8, 560–584.
Peters, A.D., Lively, C.M., 1999. The Red Queen and fluctuating epistasis: A
population genetic analysis of antagonistic coevolution. American Naturalist 154,
393–405.
Pike, N., Kingcombe, R., 2009. Antibiotic treatment leads to the elimination of
Wolbachia endosymbionts and sterility in the diplodiploid collembolan Folsomia
candida. BMC Biology 7, 54.
Poon, A., Chao, L., 2004. Drift Increases the advantage of sex in RNA bacteriophage
phi6. Genetics 166, 19–24.
Provencher, L.M., Morse, G.E., Weeks, A.R., Normark, B.B., 2005. Parthenogenesis
in the Aspidiotus nerii complex (Hemiptera: Diaspididae): A single origin of a
worldwide, polyphagous lineage associated with Cardinium bacteria. Annals of
the Entomological Society of America 98, 629–635.
Pylkov, K.V., Zhivotovsky, L., Feldman, M.W., 1998. Migration versus mutation in
the evolution of recombination under multilocus selection. Genetical Research 71,
247–256.
Song, Y., Drossel, B., Scheu, S., 2011. Tangled Bank dismissed too early. Oikos
120, 1601–1607.
Suomalainen, E., Saura, A., Lokki, J., 1987. Cytology and Evolution in
Parthenogenesis. Boca Raton, FL: CRC Press.
Tucker, A., Ackerman, M., 2013. Population-genomic insights into the evolutionary
origin and fate of obligately asexual Daphnia pulex. Proceedings of the National
Academy of Sciences of the United States of America 110, 15740–15745.
De Visser, J.A.G.M., Elena, S.F., 2007. The evolution of sex: Empirical insights into
the roles of epistasis and drift. Nature Reviews Genetics 8, 139–149.
Vrijenhoek, R.C., 1998. Animal clones and diversity. Bioscience 48, 617–628.
West, S.A., Lively, C.M., Read, A.F., 1999. A pluralist approach to sex and
recombination. Journal of Evolutionary Biology 12, 1003–1012.
Williams, G.C., 1975. Sex and Evolution. Oxford: Princeton University Press.
Wilson, A.C.C., Sunnucks, P., Hales, D.F., 1997. Random loss of X chromosome
at male determination in an aphid, Sitobion near fragariae, detected using an
X-linked polymorphic microsatellite marker. Genetical Research 69, 233–236.
Sex, Evolution and Maintenance of 97
Author's personal copy
